Structural changes in brain regions involved in executive-control and self-referential processing after sleeve gastrectomy in obese patients
Obesity-related brain gray (GM) and white matter (WM) abnormalities have been reported in regions associated with food-intake control and cognitive-emotional regulation. Bariatric surgery (BS) is the most effective way to treat obesity and induce structural recovery of GM/WM density and WM integrity. It is unknown whether the surgery can promote structural changes in cortical morphometry along with weight-loss. Structural Magnetic Resonance Imaging and surface-based morphometry analysis were used to investigate BS-induced alterations of cortical morphometry in 22 obese participants who were tested before and one month post-BS, and in 21 obese controls (Ctr) without surgery who were tested twice (Baseline and One-month). Results showed that fasting plasma ghrelin, insulin, and leptin levels were significantly reduced post-BS (P < 0.001). Post-BS there were significant decreases in cortical thickness in the precuneus (PFDR < 0.05) that were associated with decreases in BMI. There were also significant increases post-BS in cortical thickness in middle (MFG) and superior (SFG) frontal gyri, superior temporal gyrus (STG), insula and ventral anterior cingulate cortex (vACC); and in cortical volume in left postcentral gyrus (PostCen) and vACC (PFDR < 0.05). Post-BS changes in SFG were associated with decreases in BMI. These findings suggest that structural changes in brain regions implicated in executive control and self-referential processing are associated with BS-induced weight-loss.
KeywordsObesity Bariatric surgery Cortical morphometry Linear mixed effects
This work is supported by the National Natural Science Foundation of China under Grant Nos. 61431013, 81470816, 81501543, 81601563, and 81730016; National Clinical Research Center for Digestive Diseases, Xi’an, China under Grant No. 2015BAI13B07; and support in part from the Intramural Research Program of the United States National Institute on Alcoholism and Alcohol Abuse, Z01AA3009 (ESK, DT, NDV, GJW). We thank Mingzhu Xu and Long Qian for their contribution to the manuscript.
Compliance with ethical standards
Conflict of interest
The authors declare no conflict of interest.
Informed consent was obtained from all patients included in the study.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.
- Benjamini, Y., Krieger, A. M., & Yekutieli, D. (2006). Adaptive linear step-up procedures that control the false discovery rate. Biometrika, 93(3), 491–507.Google Scholar
- van de Sande-Lee, S., Pereira, F. R., Cintra, D. E., Fernandes, P. T., Cardoso, A. R., Garlipp, C. R., Chaim, E. A., Pareja, J. C., Geloneze, B., Li, L. M., et al. (2011). Partial reversibility of hypothalamic dysfunction and changes in brain activity after body mass reduction in obese subjects. Diabetes, 60(6), 1699–1704.PubMedPubMedCentralGoogle Scholar
- Desikan, R. S., Segonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., Buckner, R. L., Dale, A. M., Maguire, R. P., Hyman, B. T., et al. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage, 31(3), 968–980.PubMedGoogle Scholar
- Fischl, B., & Dale, A. M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceeding of the National Academy Sciences United States of America, 97(20), 11050–11055.Google Scholar
- Frank, S., Wilms, B., Veit, R., Ernst, B., Thurnheer, M., Kullmann, S., Fritsche, A., Birbaumer, N., Preissl, H., & Schultes, B. (2014). Altered brain activity in severely obese women may recover after roux-en Y gastric bypass surgery. International Journal of Obesity (London), 38(3), 341–348.Google Scholar
- Grosshans, M., Vollmert, C., Vollstadt-Klein, S., Tost, H., Leber, S., Bach, P., Buhler, M., von der Goltz, C., Mutschler, J., Loeber, S., et al. (2012). Association of leptin with food cue-induced activation in human reward pathways. Archives of General Psychiatry, 69(5), 529–537.PubMedGoogle Scholar
- Hamilton, M. (1959). The assessment of anxiety states by rating. British Journal of Medical Psychology, 32(1), 50–5.Google Scholar
- Hamilton, M. (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry, 23(1), 56–62.Google Scholar
- Hao, X., Xu, D., Bansal, R., Dong, Z., Liu, J., Wang, Z., Kangarlu, A., Liu, F., Duan, Y., Shova, S., Gerber, A. J., & Peterson, B. S. (2013). Multimodal magnetic resonance imaging: The coordinated use of multiple, mutually informative probes to understand brain structure and function. Human Brain Mapping, 34(2), 253–271.PubMedGoogle Scholar
- Hassenstab, J. J., Sweet, L. H., Del, P. A., McCaffery, J. M., Haley, A. P., Demos, K. E., Cohen, R. A., & Wing, R. R. (2012). Cortical thickness of the cognitive control network in obesity and successful weight loss maintenance: A preliminary MRI study. Psychiatry Research, 202(1), 77–79.PubMedPubMedCentralGoogle Scholar
- Killgore, W. D., Weber, M., Schwab, Z. J., Kipman, M., DelDonno, S. R., Webb, C. A., & Rauch, S. L. (2013). Cortico-limbic responsiveness to high-calorie food images predicts weight status among women. International Journal of Obesity (London), 37(11), 1435–1442.Google Scholar
- Lepping, R. J., Bruce, A. S., Francisco, A., Yeh, H. W., Martin, L. E., Powell, J. N., Hancock, L., Patrician, T. M., Breslin, F. J., Selim, N., Donnelly, J. E., Brooks, W. M., Savage, C. R., Simmons, W. K., & Bruce, J. M. (2015). Resting-state brain connectivity after surgical and behavioral weight loss. Obesity (Silver Spring), 23(7), 1422–1428.Google Scholar
- Li, C. S., Morgan, P. T., Matuskey, D., Abdelghany, O., Luo, X., Chang, J. L., Rounsaville, B. J., Ding, Y. S., & Malison, R. T. (2010). Biological markers of the effects of intravenous methylphenidate on improving inhibitory control in cocaine-dependent patients. Proceeding of the National Academy Sciences United States of America, 107(32), 14455–14459.Google Scholar
- Makaronidis, J. M., & Batterham, R. L. (2018). Obesity, body weight regulation and the brain: Insights from fMRI. British Journal of Radiology. https://doi.org/10.1259/bjr.20170910.
- Marques-Iturria, I., Pueyo, R., Garolera, M., Segura, B., Junque, C., Garcia-Garcia, I., Jose, S. M., Vernet-Vernet, M., Narberhaus, A., Ariza, M., et al. (2013). Frontal cortical thinning and subcortical volume reductions in early adulthood obesity. Psychiatry Research, 214(2), 109–115.PubMedGoogle Scholar
- Medic, N., Ziauddeen, H., Ersche, K. D., Farooqi, I. S., Bullmore, E. T., Nathan, P. J., Ronan, L., & Fletcher, P. C. (2016). Increased body mass index is associated with specific regional alterations in brain structure. International Journal of Obesity (London), 40(7), 1177–1182.Google Scholar
- Navas, J. F., Barros-Loscertales, A., Costumero-Ramos, V., Verdejo-Roman, J., Vilar-Lopez, R., & Verdejo-Garcia, A. (2017). Excessive body fat linked to blunted somatosensory cortex response to general reward in adolescents. International Journal of Obesity (London), 42, 88–94.Google Scholar
- Tuulari, J. J., Karlsson, H. K., Antikainen, O., Hirvonen, J., Pham, T., Salminen, P., Helmio, M., Parkkola, R., Nuutila, P., & Nummenmaa, L. (2016). Bariatric surgery induces white and Grey matter density recovery in the morbidly obese: A voxel-based morphometric study. Human Brain Mapping, 37(11), 3745–3756.PubMedGoogle Scholar
- Vidal, P., Ramon, J. M., Goday, A., Benaiges, D., Trillo, L., Parri, A., Gonzalez, S., Pera, M., & Grande, L. (2013). Laparoscopic gastric bypass versus laparoscopic sleeve gastrectomy as a definitive surgical procedure for morbid obesity. Mid-term results. Obesity Surgery, 23(3), 292–299.PubMedGoogle Scholar
- Vitaglione, P., Mennella, I., Ferracane, R., Rivellese, A. A., Giacco, R., Ercolini, D., Gibbons, S. M., La Storia, A., Gilbert, J. A., Jonnalagadda, S., et al. (2015). Whole-grain wheat consumption reduces inflammation in a randomized controlled trial on overweight and obese subjects with unhealthy dietary and lifestyle behaviors: Role of polyphenols bound to cereal dietary fiber. American Journal of Clinical Nutrition, 101(2), 251–261.PubMedGoogle Scholar
- Wallis, C. U., Cardinal, R. N., Alexander, L., Roberts, A. C., & Clarke, H. F. (2017). Opposing roles of primate areas 25 and 32 and their putative rodent homologs in the regulation of negative emotion. Proceeding of the National Academy Sciences United States of America, 114(20), E4075–E4084.Google Scholar
- Wiemerslage, L., Zhou, W., Olivo, G., Stark, J., Hogenkamp, P. S., Larsson, E. M., Sundbom, M., & Schioth, H. B. (2017). A resting-state fMRI study of obese females between pre- and postprandial states before and after bariatric surgery. European Journal of Neuroscience, 45(3), 333–341.PubMedGoogle Scholar
- Yokum, S., & Stice, E. (2013). Cognitive regulation of food craving: Effects of three cognitive reappraisal strategies on neural response to palatable foods. International Journal of Obesity (London), 37(12), 1565–1570.Google Scholar
- Zhang, Y., Ji, G., Xu, M., Cai, W., Zhu, Q., Qian, L., Zhang, Y. E., Yuan, K., Liu, J., Li, Q., Cui, G., Wang, H., Zhao, Q., Wu, K., Fan, D., Gold, M. S., Tian, J., Tomasi, D., Liu, Y., Nie, Y., & Wang, G. J. (2016). Recovery of brain structural abnormalities in morbidly obese patients after bariatric surgery. International Journal of Obesity (London), 40(10), 1558–1565.Google Scholar